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Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)

Two orthologues of the gene encoding the Na(+)-Cl(−) cotransporter (NCC), termed ncca and nccb, were found in the sea lamprey genome. No gene encoding the Na(+)-K(+)-2Cl(−) cotransporter 2 (nkcc2) was identified. In a phylogenetic comparison among other vertebrate NCC and NKCC sequences, the sea lam...

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Autores principales: Barany, A., Shaughnessy, C. A., Pelis, R. M., Fuentes, J., Mancera, J. M., McCormick, S. D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8608846/
https://www.ncbi.nlm.nih.gov/pubmed/34811419
http://dx.doi.org/10.1038/s41598-021-02125-1
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author Barany, A.
Shaughnessy, C. A.
Pelis, R. M.
Fuentes, J.
Mancera, J. M.
McCormick, S. D.
author_facet Barany, A.
Shaughnessy, C. A.
Pelis, R. M.
Fuentes, J.
Mancera, J. M.
McCormick, S. D.
author_sort Barany, A.
collection PubMed
description Two orthologues of the gene encoding the Na(+)-Cl(−) cotransporter (NCC), termed ncca and nccb, were found in the sea lamprey genome. No gene encoding the Na(+)-K(+)-2Cl(−) cotransporter 2 (nkcc2) was identified. In a phylogenetic comparison among other vertebrate NCC and NKCC sequences, the sea lamprey NCCs occupied basal positions within the NCC clades. In freshwater, ncca mRNA was found only in the gill and nccb only in the intestine, whereas both were found in the kidney. Intestinal nccb mRNA levels increased during late metamorphosis coincident with salinity tolerance. Acclimation to seawater increased nccb mRNA levels in the intestine and kidney. Electrophysiological analysis of intestinal tissue ex vivo showed this tissue was anion absorptive. After seawater acclimation, the proximal intestine became less anion absorptive, whereas the distal intestine remained unchanged. Luminal application of indapamide (an NCC inhibitor) resulted in 73% and 30% inhibition of short-circuit current (I(sc)) in the proximal and distal intestine, respectively. Luminal application of bumetanide (an NKCC inhibitor) did not affect intestinal I(sc). Indapamide also inhibited intestinal water absorption. Our results indicate that NCCb is likely the key ion cotransport protein for ion uptake by the lamprey intestine that facilitates water absorption in seawater. As such, the preparatory increases in intestinal nccb mRNA levels during metamorphosis of sea lamprey are likely critical to development of whole animal salinity tolerance.
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spelling pubmed-86088462021-11-24 Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus) Barany, A. Shaughnessy, C. A. Pelis, R. M. Fuentes, J. Mancera, J. M. McCormick, S. D. Sci Rep Article Two orthologues of the gene encoding the Na(+)-Cl(−) cotransporter (NCC), termed ncca and nccb, were found in the sea lamprey genome. No gene encoding the Na(+)-K(+)-2Cl(−) cotransporter 2 (nkcc2) was identified. In a phylogenetic comparison among other vertebrate NCC and NKCC sequences, the sea lamprey NCCs occupied basal positions within the NCC clades. In freshwater, ncca mRNA was found only in the gill and nccb only in the intestine, whereas both were found in the kidney. Intestinal nccb mRNA levels increased during late metamorphosis coincident with salinity tolerance. Acclimation to seawater increased nccb mRNA levels in the intestine and kidney. Electrophysiological analysis of intestinal tissue ex vivo showed this tissue was anion absorptive. After seawater acclimation, the proximal intestine became less anion absorptive, whereas the distal intestine remained unchanged. Luminal application of indapamide (an NCC inhibitor) resulted in 73% and 30% inhibition of short-circuit current (I(sc)) in the proximal and distal intestine, respectively. Luminal application of bumetanide (an NKCC inhibitor) did not affect intestinal I(sc). Indapamide also inhibited intestinal water absorption. Our results indicate that NCCb is likely the key ion cotransport protein for ion uptake by the lamprey intestine that facilitates water absorption in seawater. As such, the preparatory increases in intestinal nccb mRNA levels during metamorphosis of sea lamprey are likely critical to development of whole animal salinity tolerance. Nature Publishing Group UK 2021-11-22 /pmc/articles/PMC8608846/ /pubmed/34811419 http://dx.doi.org/10.1038/s41598-021-02125-1 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Barany, A.
Shaughnessy, C. A.
Pelis, R. M.
Fuentes, J.
Mancera, J. M.
McCormick, S. D.
Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)
title Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)
title_full Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)
title_fullStr Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)
title_full_unstemmed Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)
title_short Tissue and salinity specific Na(+)/Cl(−) cotransporter (NCC) orthologues involved in the adaptive osmoregulation of sea lamprey (Petromyzon marinus)
title_sort tissue and salinity specific na(+)/cl(−) cotransporter (ncc) orthologues involved in the adaptive osmoregulation of sea lamprey (petromyzon marinus)
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8608846/
https://www.ncbi.nlm.nih.gov/pubmed/34811419
http://dx.doi.org/10.1038/s41598-021-02125-1
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